Surveys for natural enemies of giant hogweed ( mantegazzianum) in the Caucasus region and assessment for their classical biological control potential in Europe

Marion K. Seier,1 Rüdiger Wittenberg,2 Carol A. Ellison,1 Djamila H. Djeddour1 and Harry C. Evans1

Summary () (giant hogweed), a biennial or perennial herb indigenous to the Caucasus mountains, has become an important invasive alien weed throughout Europe as well as in parts of North America. First introduced into botanical gardens in central and northern Europe in the late 1800s, H. mantegazzianum was subsequently widely planted as an ornamental and has now become invasive in most of its introduced range in western Europe. Giant hogweed not only replaces the native flora and alters ecosystems along waterways, but also poses a risk to human health by causing after contact with its sap. In January 2002, a collaborative European Union-funded program was initiated aiming to develop an integrated strategy for management of H. mantegazzianum in its exotic range. Biological control forms a central theme in this program and a series of surveys for both and pathogen natural enemies are being undertaken in the Caucasus region. The initial surveys have revealed an extensive mycobiota associated with H. mantegazzianum, most species of which are new records for this host. At least four, purportedly co-evolved pathogens belonging to the genera Ramulariopsis, Septoria, Phloe- ospora and Phoma were collected, of which the first three are under evaluation regarding their potential as biological control agents. The most prominent phytophagous present on H. mantegazzinanum was found to be the stem-boring curculionid Lixus iridis. Other collected attacked different parts of the host : Diptera species in the roots, Lepidoptera feeding on the leaves and flowers, and thrips species sucking on leaves, stems and flower heads. Likewise, the potential of these insect agents is currently being assessed.

Keywords: biological control, Caucasus, fungal pathogens, Heracleum mantegazzianum, phytophagous insects.

Introduction stretching from the Black Sea to the Caspian Sea, the plant was first introduced into botanical gardens in Heracleum mantegazzianum Somm. & Lev., central and northern Europe in the late 19th century commonly known as giant hogweed, is a biennial or (Briggs 1979, Lundström 1984). With its impressive perennial herb belonging to the Apiaceae. Native to the height of up to 5 metres and its large showy leaves and western part of the Caucasus, the mountain range flowerheads, H. mantegazzianum was subsequently promoted by nurseries and actively planted as an orna- mental curiosity in large private gardens and parks. 1 CABI Bioscience UK Centre, Silwood Park, Ascot, Berkshire, SL5 7TA, UK. Since then, the plant has escaped, spreading naturally 2 CABI Bioscience Switzerland Centre, 1 Rue des Grillons, CH-2800 by seed propagation, with each individual potentially Delémont, Switzerland. producing up to 120,000 seeds per year (Dodd et al. Corresponding author: Marion Seier, CABI Bioscience UK Centre, Silwood Park, Ascot, Berkshire, SL5 7TA, UK. [email protected] 1994). The initial spread occurred mainly along rivers

149 Proceedings of the XI International Symposium on Biological Control of Weeds and streams, affecting riparian habitats (Caffrey 1994; has been considered as an alternative or additional Dodd et al. 1994). However, due to human activities, H. strategy for the management of giant hogweed, little mantegazzianum has colonized a variety of habitats research has been undertaken in this field to date such as agricultural land, abandoned fields, and road (Sampson 1990, 1994, Fowler et al. 1991, Caffrey 1994). and railway embankments, as well as urban sites (Pys˘ek The need to develop an integrated management 1994, Tiley et al. 1996). It is now a widespread weed in strategy that comprises effective, practicable and sustain- most of its introduced European range as well as in able means to control the spread of H. mantegazzianum parts of North America (Morton 1978). in its introduced European range, led to the initiation of Rapid growth and a large leaf area forming dense a collaborative multidisciplinary project funded by the canopies makes giant hogweed highly competitive and European Union in January 2002. Biological control, capable of shading out native herbaceous species, thus particularly the evaluation of co-evolved natural enemies posing a significant threat to the local biodiversity and from the native range of the plant as classical biocontrol altering whole ecosystems (Vogt Andersen 1994, agents, forms a central theme of this project. Pys˘ek & Pys˘ek 1995, Otte & Franke 1998). Following its annual winter die-back the weed exposes large areas Materials and methods of bare ground leaving the soil vulnerable to erosion, especially along riverbanks (Williamson & Forbes 1982). The sap, which is present in all parts of H. Field surveys mantegazzianum, contains a number of furanocumarins Two field trips were undertaken to the Russian part giving it photosensitizing properties (Hipkin 1991). of the Caucasus mountains to establish the mycobiota Skin contact with the plant causes severe blistering and and herbivore fauna associated with H. mante- dermatitis in affected humans, making the plant a gazzianum in its native range and to assess the damage serious public health hazard, especially when growing caused by individual fungal and arthropod species to in amenity areas (Dodd et. al. 1994). this host, as well as to related plant species. The surveys Current methods of control are based on herbicide were undertaken at the beginning of June and July application, particularly as glyphosate, grazing 2002, respectively, covering 11 field sites between and mechanical control, such as cutting and ploughing Pyatigorsk in the east and the Krasnodar territory in the (Dodd et al., 1994, Lundström & Darby 1994). However, west. The altitude of these sites ranges from 510 to overall, these methods have failed to give lasting control 1670 m.a.s.l. A map showing the location of individual of the weed (Sampson 1994). While biological control field sites is given in Figure 1.

Figure 1. Map showing the sites surveyed ( ) in the Caucasus region in 2002. (ref. http://caspian.hypermart.net/caucasus.gif)

150 Natural enemies of Heracleum mantegazzianum

Fungal pathogens length of the longest leaf, number of flower heads and the diameter of the central flower head. Observations of At each field site, a representative number of H. phytophagous insects on and in these parts of the plant mantegazzianum and related species was were also noted. Each plant was dug out completely and assessed, comprising all ages of plants present. Level all stems, petioles, and roots were dissected. In addition and type of pathogen damage was recorded and to these randomly chosen plants, as many plants as samples were taken. These were brought back in a plant possible were assessed for signs of insect attack. press into the quarantine facilities at CABI Bioscience All stages of insects found were collected together UK Centre where all subsequent work was carried out. with pieces of the plant parts, where they were feeding, Suspected biotrophic pathogens were isolated immedi- and kept in plastic boxes. When necessary, plant material ately onto H. mantegazzianum plants grown from seeds was replaced with fresh material. The samples were trans- ex Kew Botantical Gardens, purportedly obtained from ported into quarantine at the CABI Switzerland Centre, original plant collections in the Caucasus. Facultative where they were transferred onto potted plants. Adults pathogens were isolated onto potato carrot agar. A emerging out of the rearing cages are being identified. representative range of fungal specimens was taxonom- ically identified and deposited either in the culture As with fungal pathogens, initial host-specificity collection or the dried reference collection of the CABI tests were carried out using the following closely Bioscience fungal herbarium (Herb. IMI). related native and economically important plants: cori- ander, carrot, Foeniculum vulgare Miller () and Plant inoculations with fungal pathogens were Heracleum sphondylium L. The adult feeding and undertaken using spores obtained either from infected oviposition tests were carried out under single-choice plant material or from agar cultures. Spore suspensions as well as multiple-choice conditions, using potted in sterile distilled water containing 0.01% Tween 80 plants in cages. All plants were examined for feeding were applied to leaf surfaces of H. mantegazzianum at traces and dissected for eggs. a concentration of 106 spores ml–1 using a fine paint- brush. Either both upper and lower leaf surfaces were treated, or exclusively one or the other. Inoculated Results plants were placed in a dew chamber (Mercia Scien- tific, Birmingham, UK) for two days at 16°C and were Fungal pathogens subsequently maintained in a controlled environment room at 20°C, with a light regime of 12h light/12h dark. An extensive mycobiota was found to be associated Treated plants were regularly assessed for the develop- with H. mantegazzianum in its native Caucasus region, ment of macroscopic symptoms of infection, and with a number of species newly recorded from this host. disease development was closely monitored and At least four potentially co-evolved pathogens were recorded. found during the early season survey (June), though Initial host-specificity studies were conducted using their overall abundance was very low. These pathogens the following test plant species belonging to the same were subsequently identified and deposited as: Septoria subfamily (Apioideae) within the Apiaceae as H. heracleicola Kabát & Bubák (Herb. IMI no. 389651); mantegazzianum: L. (angelica), Ramulariopsis sp. nov. (Herb. IMI nos. 389652, Coriandrum sativum L. (coriander), Daucus carota L. 389653, 389656); Phoma sp. (possibly Phoma longis- (carrot), Ferula communis L. (giant fennel) and Pasti- sima (Pers.)Westend. (Herb. IMI no. 389654)); Phloe- naca sativa L. (). Three plants were tested per ospora heraclei (Lib.) Petr (Herb. IMI nos. 389658, species and a range of different leaf stages was inocu- 389659). By mid season (July 2002) some additional lated. Inoculations and the subsequent maintenance of fungal species, identified as Ramularia heraclei treated plants were carried out as outlined above. A test (Oudem.) Sacc. (Herb. IMI no. 389655) and Erysiphe run was regarded as positive once the pathogen sporu- heraclei DC. (not deposited), were recorded. It was lated on the three inoculated plants of H. mante- noted that the abundance of all pathogens had markedly gazzianum included as positive controls. Individual test increased both on first year and mature plants. The plant species were closely monitored for the develop- genera Phloeospora and Ramulariopsis were also ment of any disease symptoms related to the respective found on related Heracleum species and the inter-rela- fungal agent for at least double the period of time tionships are being investigated. Further evaluations of required by the pathogen to sporulate on its host. P. heraclei (Herb. IMI 389658), S. heracleicola and Ramulariopsis sp. nov. (Herb. IMI 389652) have commenced under quarantine conditions in the UK. Herbivores Field observations indicated that the coelomycete Plants were taken at random and dissected according fungus P. heraclei might have a high potential as a to a protocol developed beforehand. Besides general data biocontrol agent since it occurred at all sites, causing about the field site, selected parameters of the plants significant damage in the form of leafspot and die-back were recorded in datasheets: plant height, diameter of the to H. mantegazzianum plants of all ages, and particu- stem, diameter of the root, number of leaves and the larly to plants at the seedling stage. Laboratory studies

151 Proceedings of the XI International Symposium on Biological Control of Weeds revealed P. heraclei to be a true biotroph or obligate feeding on the outer parts of the root may be sapro- parasite since it could be cultured only on its living phytic. The most obvious phytophagous insect present host. Infection of H. mantegazzianum occurs through on the plants was Lixus iridis Ol. (), the lower leaf surface leading to chlorotic spots ca. 7 which was found on most sites, with a high abundance days after inoculation and subsequent sporulation ca. at some sites. It was not uncommon to find 10 larvae in 2–3 days later. The pathogen forms conspicuous large one stem. The adults mate on the highest parts of the pale brown acervuli bearing hyaline, curved conidia on plants and, after copulation, eggs are laid inside the the upper leaf surface of its host. These are associated hollow stem. Dissections and field observation of the with black crusts, considered to represent either feeding adults show that eggs and larvae occur mainly in the or survival structures, forming on the lower leaf stem, but also in the larger petioles of the leaves. Adults surface. Under controlled environment conditions, and eggs of this were also recorded on another infection of H. mantegazzianum with P. heraclei was Heracleum sp. (most probably Heracleum asperum consistently high. Initial host specificity studies (Hoffm.) M. Bieb.) during the survey. Some 74 adults showed that P. heraclei can sporadically infect parsnip were brought back into quarantine at the Centre. and coriander, showing restricted sporulation with Besides these root and stem-feeding insects, some smaller pustules than those formed on H. mante- unidentified leaf-feeding larvae were found, especially gazzianum. To date, no symptoms have been recorded in the western part of the surveyed area. Two thrips on the test plant species angelica, carrot and giant species were found in very high numbers on H. mante- fennel. gazzianum, one feeding on the leaves and the other on Septoria heracleicola closely resembles P. heraclei, the stems and flower/seed heads. The latter species had both in the disease symptoms caused as well as in a dramatic impact on the development of flowers on macromorphology. In the field, mixed infections of single plants. Unfortunately, it was subsequently deter- both pathogens were frequently encountered on H. mined as the rather polyphagous Thrips vulgatissimus mantegazzianum, with P. heraclei being the dominant (Haliday). Depressaria spp. (Oecophoridae) larvae agent. Therefore, an accurate assessment of the impact were found feeding within the flower heads. of S. heracleicola on its host alone is still lacking. Preliminary host-range testing with L. iridis showed Septoria heracleicola can easily be cultured in vitro and that they did not feed or oviposit on three plants of produces infective conidia. Inoculation using conidia economic importance, i.e. coriander, carrot and fennel, from agar culture leads to the formation of necrotic leaf under single as well as multiple-choice conditions. spots on H. mantegazzianum after ca. 15 days. Sporula- However, during the tests only nine eggs were found on tion on these necrotic lesions could be induced by incu- H. mantegazzianum, but feeding was recorded on bation in a humid chamber for two days. Initial studies almost all host plant replicates. showed that H. mantegazzianum is susceptible to S. A previously undetermined noctuid larvae feeding heracleicola under controlled environment conditions. gregariously on the leaves of H. mantegazzianum in the A preliminary assessment of the host specificity of this Caucasus, was also used in preliminary host-range pathogen has commenced and the results are pending. testing. After adult emergence, the species was identi- The cercosporoid fungus Ramulariopsis sp. nov. is a fied as Mamestra brassicae (L.) Barathra, a well known hitherto undescribed species and is the first record of pest on Brassica spp. In single-choice tests the larvae the genus Ramulariopsis for the family Apiaceae (J.C. fed on all the test plants offered. David, pers. comm.). It remains to be established whether the different specimens deposited in the culture collection of the CABI Bioscience herbarium Discussion represent isolates of the same species. The pathogen In order to develop an integrated strategy for manage- causes angular lesions with a distinct cottony appear- ment of H. mantegazzianum in Europe, biological ance once sporulation occurs. Its impact on H. mante- control needs to be considered as one approach, poten- gazzianum in the field can be variable. Ramulariopsis tially contributing to long-term control of the weed. sp. nov. produces infective conidia in vitro and initial Areas with restricted infestations of giant hogweed can pathogenicity studies have shown that the first symp- be effectively managed employing mechanical and toms of disease, seen as necrotic lesions on infected chemical control, but the only sustainable solution for leaves, appear ca. 10 days after inoculation. The path- large populations of the weed would be classical ogen sporulates predominantly on the lower leaf biological control. While a range of herbivores and surface of its host. fungal pathogens has been recorded from giant hogweed in its exotic distribution, these comprise Herbivores mainly polyphagous insect species, which generally While there were no feeding traces on any of the have little impact on the plant; and generalist patho- roots during the first survey in June 2002, Diptera gens, usually exhibiting a relatively wide host range larvae were found to mine the roots later in July. The (Sampson 1990, Bürki & Nentwig 1998). Hence, such species have not yet been identified and some of them insect and fungal species are considered to have little or

152 Natural enemies of Heracleum mantegazzianum no potential as biological control agents. In contrast, In 2003, additional surveys will be undertaken both knowledge about the natural enemy complex that co- in the invasive and the native range of H. mante- evolved with H. mantegazzianum in its native Caucasus gazzianum in order to complete the inventory of fungal range is still scarce. The recent survey work docu- pathogens and herbivores associated with this host. It is mented here has established that a diverse mycobiota hoped that further visits in the Caucasus at different and herbivore complex is associated with giant times of the year and other field sites will reveal addi- hogweed in its centre of origin, with a number of tional agents for further studies. species constituting first records for this host. Phloeospora heraclei appears to have high potential Acknowledgements as a biological control agent due to its impact on H. mantegazzianum. Being particularly damaging to H. These studies were supported by European Union mantegazzianum at the seedling stage, the pathogen funding under the 5th Framework program “EESD – would affect the weed at a critical phase of its life cycle Energy, Environment and Sustainable Development”; given the inability of giant hogweed to spread vegeta- project number EVK2-2001-00125. Scientists of the tively (Ochsmann 1996). However, the host specificity Russian Academy of Sciences (St. Petersburg and Pyat- of P. heraclei will need to be critically evaluated given igorsk), particularly Dmitry Geltman, Boris Zhitar, its apparent ability to infect non-target species, such as Svyatoslav Bondarenko, Tatyana Volkovich, Vladimir parsnip and coriander, under controlled environment Lantsov and Sergey Ya. Reznik provided scientific and conditions. Artificial host range extension of plant logistical support during the surveys and we acknowl- pathogens in greenhouse screening is a well-docu- edge their invaluable assistance. Wolfgang Nentwig, mented phenomenon (Cother 1975, Evans 1995) and Steen Ole Hansen and Jan Hattendorf from the Zoolog- restricted sporulation, as seen for P. heraclei on these ical Institute, University of Bern, Switzerland, partici- test species, is generally viewed as an expression of pated in the surveys. Special thanks go to Travis plant resistance (Heath 1982). However, records in the Turner, who helped with rearing and specificity testing CABI Bioscience fungal herbarium revealed that P. of the insects in quarantine, as well as to Sue Paddon heraclei has been reported from parsnip as well as from who provided the plant material for the pathogen work. the indigenous H. sphondylium in the UK and other European countries. The incidence of P. heraclei on References these hosts reported from Europe, as well as a potential presence of the pathogen on H. mantegazzianum in its Briggs, M. (1979) Giant hogweed – a poisonous plant. BSBI exotic range, has to be established and pathogen strains News 21, 27–28. from different hosts and regions need to be character- Bürki, C. & Nentwig, W. (1998) Comparison of herbivore ized and compared. insect communities of Heracleum sphondylium and Regarding the other two fungal pathogens currently H. mantegazzianum in Switzerland (Spermatophyta: Apiaceae). Entomologia-Generalis 22 (2), 147–155. under evaluation, S. heracleicola and the cercosporiod Caffrey, J.M. (1994) Spread and management of Heracleum fungus Ramulariopsis sp. nov., their impact on mantegazzianum (Giant Hogweed) along Irish river corri- H. mantegazzianum needs to be determined and their dors. Ecology and Management of Invasive Riverside Plants host specificity assessed. Fungal pathogens belonging to (eds L.C. de Waal, L.E. Child, P.M. Wade & J.H. Brock), the genus Septoria as well as other cercosporoid fungi pp. 67–76. 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